Wednesday, July 23, 2014

Evolutionary fitness and incest

I have written before about the expected genetic problems associated with inbreeding, including consanguinity and incest (relationships between people who are first cousins or closer). Conventionally, the evolutionary advantage of sexual over non-sexual reproduction is considered to be the creation of genetic diversity through heterozygosity. Inbreeding, by reducing heterozygosity, then seems to negate the advantages of sexual reproduction — it leads to the propagation of deleterious recessive alleles and thus inbreeding depression. So, there is a clear evolutionary dimension to the fact that incest avoidance is nearly universal in humans.

The best known exceptions to this situation are among royalty, including the family "trees" of the ancient Egyptian 18th Dynasty (see Tutankhamun and extreme consanguinity) and the Egyptian Ptolemaic dynasty (see Cleopatra, ambition and family networks), which were hybridization networks rather than conventional trees. The presence of consanguinity and incest among royal families then requires a biological explanation. As noted by van den Berghe & Mesher (1980):

Royal incest is best explained in terms of the general sociobiological paradigm of inclusive fitness ... Royal incest (mostly brother-sister; less commonly father-daughter) represents the logical extreme of hypergyny. Women in stratified societies maximize fitness by marrying up; the higher the status of a woman, the narrower her range of prospective husbands. This leads to a direct association between high status and inbreeding.

The benefits of inclusive fitness refer to the increased number of offspring in future generations that result from increasing the reproductive success of close relatives. This is achieved via choice of mate. In other words, close relatives share genes, and the success of any relative in leaving offspring is a success for all relatives. Therefore, evolutionary fitness is a combination of individual fitness plus the fitness of close relatives. Inbreeding may reduce individual fitness but can increase inclusive fitness, as noted by Puurtinen (2011):

Theoretical work has shown that inclusive fitness benefits can favor close inbreeding even when this results in substantial reduction in offspring fitness. These models have identified the boundary level of inbreeding depression limiting the evolution of inbreeding among first-order relatives, that is, between full siblings, or between parents and offspring.

So, there is a stable level of inbreeding in those populations that practice mate choice for optimal inbreeding. For example, the genetic risks of close inbreeding can be more than accounted for by the production of a highly related heir who has access to a wide choice of mates. Nevertheless:

In other words, mating with very close relatives is unlikely to evolve via natural selection because it is not an optimal strategy; and we must thus look to a sociological component to incest (such as retaining wealth within the family), as well as a biological one.

In this context, it is interesting to note exceptions to the usual restriction of incest to the aristocracy. The society of Graeco-Roman Egypt (from c. 300 BCE to 300 CE) provides the best-documented case (eg. see Hopkins 1980; Shaw 1992; Parker 1996; Scheidel 1997; Huebner 2007; Remijsen & Clarysse 2008). [This era starts with the Ptolemaic dynasty, which marks the collapse of Egyptian rule of Egypt.] During this time a significant proportion of all marriages noted in official Roman census declarations were between full brothers and sisters. That is, the Roman-era Egyptians did not limit this type of inbreeding to any small group, but spread it across several social classes (mainly Greek settlers rather than native Egyptians).

As noted by Schiedel (1997):

According to official census returns from Roman Egypt (first to third centuries CE) preserved on papyrus, 23·5% of all documented marriages in the Arsinoites district in the Fayum (n=102) were between brothers and sisters. In the second century CE, the rates were 37% in the city of Arsinoe and 18·9% in the surrounding villages. Documented pedigrees suggest a minimum mean level of inbreeding equivalent to a coefficient of inbreeding of 0·0975 in second century CE Arsinoe. Undocumented sources of inbreeding and an estimate based on the frequency of close-kin unions indicate a mean coefficient of inbreeding of F=0·15-0·20 in Arsinoe and of F=0·10-0·15 in the villages at the end of the second century CE. These values are several times as high as any other documented levels of inbreeding.

However, inbreeding depression seems not to have been a notable problem during this historical time. As noted by John Hawkes:

There is not a single mention in the evidence that links sibling marriage to negative genetic effects or unhappy marriages.

This does not mean that there were no problems, but merely that any problems were not documented, as noted by Scheidel (1997):

Even in the absence of explicit references to inbreeding depression from Roman Egypt, there is no compelling reason to assume that brother–sister marriage could have remained entirely without negative consequences for the Arsinoites. It is however possible that, due to a low incidence of lethal recessives, such effects were considerably weaker than in some western samples. The census returns do not suggest lower levels of fertility or smaller numbers of children among sibling couples ...

The practice seems to have stopped solely because it was contrary to Roman Law:

Before a.d. 212 the Romans had accepted discrepancies between their own legal practice and prevailing local customs and traditions in the Eastern provinces. Papyri from Roman Egypt, the Talmud, and the Romano-Syrian law book indeed reveal legal procedures which differed significantly from Roman law in matters such as marriage, guardianship, paternal authority, sales, and debts. The Constitutio Antoniana, however, made all free men and women of the Roman Empire into Roman citizens, and so Roman law became applicable to all inhabitants of Egypt. Brother-sister marriages cease to be documented in our Roman census returns from the early third century on. Our last [incest] testimony dates to a.d. 229.